A popular Sunday morning television news show aired a segment on January 15, 2014, that provided helpful advice about a concerning outbreak of “nightmare bacteria” that had been linked just weeks earlier to a medical procedure performed on more than 200 patients seeking care at a hospital near Chicago, IL.

Entitled “Troubling outbreak of drug-resistant bacteria a growing threat,” this news segment aired on Fox News’ “Sunday Housecall” click here to watch it.

This is inexcusable that our hospitals would allow bacteria like that to grow.” —- Jamie Colby, Fox News.

One of this news segment’s statements, respectfully, warrants clarification, however, lest the insidiousness of this unprecedented bacterial outbreak possibly be otherwise overlooked.

Article’s shortcuts:  (1) The CDC’s investigation;  (2) “A ‘pocket’ outbreak?“;  (3) Multiple published reports of CRE outbreaks following ERCP;  (4) Conclusions, summary and recommendations;  (5) An unresolved issue: CRE-contaminated rinse water?

Advocate Lutheran General Hospital (Park Ridge, IL) reported in 2013 that it had recently, and unprecedentedly, notified 243 patients of their potential infection with a “superbug” (so named primarily because of its resistance to several types of antibiotics) called carbapenem-resistant Enterobacteriaceae, or “CRE.”

Just published:  Click here to download a free copy of Dr. Muscarella’s just-published article: “Risk of transmission of carbapenem-resistant Enterobacteriaceae and related ‘superbugs’ during gastrointestinal endoscopy” (World J Gastrointest Endosc 2014; 6[10]:457-474).

These 243 patients were told by hospital officials to return to be screened for infection with CRE, because of concerns that each of these “at risk” patients may have been exposed to a routinely used medical instrument contaminated with this superbug while having undergone a certain gastrointestinal (GI) procedure called endoscopic retrograde cholangiopancreatography, or “ERCP,” at this hospital between January, 2013, and September, 2013.

Of these 243 patients, over 100 returned to the hospital to be tested, and — representing the largest outbreak of this type of superbug in U.S. history, to date — 38 were found to be either infected or colonized with CRE. (Colonization, as opposed to infection, is defined as someone who carries the bacterium, but does not display clinical symptoms of infection.)

More of the details of Advocate Lutheran General Hospital’s CRE outbreak are provided in a number of articles, also written by Lawrence F Muscarella, PhD, that are listed on the Web-page entitled “Superbugs & Endoscopy” — click here.

Briefly, ERCP is often performed to diagnose and treat biliary and pancreatic diseases, and the suspect medical instrument found to be contaminated with CRE is called, not surprisingly, an “ERCP endoscope.”

(Note: While the model of ERCP endoscope that Advocate Lutheran General Hospital implicated during this outbreak’s investigation was reported to be of one specific manufacturer, the GI endoscopes of other manufacturers, too, have been linked to recent CRE outbreaks.)

Superbugs and ERCP: Click here to read a list of all of Dr. Muscarella’s articles about Advocate Lutheran General Hospital’s “superbug” outbreak in 2013.

The CDC’s investigation 

As reported by the Centers for Disease Control and Prevention (CDC) in the January 3, 2014, issue of MMWR (click here), the specific strain that was the cause of Advocate Lutheran General Hospital’s CRE outbreak is called New Delhi Metallo-β-Lactamase–Producing Escherichia coli — or “NDM-producing E. coli,” so named because it was first identified in 2009 in an infected patient seeking care at a hospital in New Delhi, India.

The CDC reported in this same MMWR report that, despite their being important to performing ERCP effectively, the complex physical design and features of the suspect ERCP endoscope model may have been responsible for Advocate Lutheran General Hospital’s superbug outbreak, stating that:

Previous studies have shown an association between ERCP endoscopes and transmission of multi-drug resistant bacteria; the design of the ERCP endoscopes might pose a particular challenge for cleaning and disinfection. — The Centers for Disease Control and Prevention.

Specifically, the CDC reports that staffers manually cleaned the hospital’s ERCP endoscopes, followed next by their high-level disinfection using an automated endoscope reprocessor, or “AER.”

Nevertheless, the CDC further reports that the elevator channel of one of these ERCP endoscopes, which was used on several of the infected (or colonized) patients, remained contaminated with NDM-producing E. coli (the outbreak’s specific strain of CRE), as well as with another strain of CRE called Klebsiella pneumoniae carbapenemase-producing Klebsiella pneumoniae, or “KPC-producing K. pneumoniae” for short.

This CRE outbreak at Advocate Lutheran General Hospital in 2013 is discussed in a peer-reviewed article by Dr. Muscarella entitled: “Risk of transmission of carbapenem-resistant Enterobacteriaceae and related ‘superbugs’ during gastrointestinal endoscopy” (World J Gastrointest Endosc 2014; 6[10]:457-474) –  click here.

“A ‘pocket’ outbreak?”

As if a moment of “deja vu,” however, these findings by the CDC caught the attention of this article’s author (Dr. Muscarella), because he had remembered recently reading about one or two, and possibly more, similar instances of CRE outbreaks following GI endoscopy, with the circumstances of each being virtually identical to those of Advocate Lutheran General Hospital’s CRE outbreak in 2013.

Which is why a comment by one of the experts during Fox News’ aforementioned “Sunday Housecall” television segment further piqued Dr. Muscarella’s  concern.  According to this news program’s expert physician:

The good news is, this is only a ‘pocket” infection in Chicago and has not yet become a systemic problem across the nation. — Fox News

Dr. Muscarella respectfully disagrees.  (For the reader’s convenience, Dr. Muscarella’s complete review of Fox News’ “Sunday Housecall” (January 15, 2014) news program discussing Advocate Lutheran General Hospital’s CRE outbreak following ERCP in 2013 is provided in his article: “Response to a News Report about a “Superbug” Outbreak in 2013 at an Illinois Hospital” — click here.

Attention Medical Device Manufacturers:  Could your reusable medical device be harboring a “superbug”? Click here to read about a quality program designed by this article’s author – Dr. Muscarella – to improve the design of reusable medical instruments and to minimize the likelihood of their association with disease transmission.

Multiple reports of CRE outbreaks following ERCP

To be sure, Advocate Lutheran General Hospital’s outbreak of the superbug CRE is anything but an isolated or singular “pocket” of infection.

A review of the literature reveals that — like a scene from the movie “Groundhog Day,” with the same day or event repeating itself — more than ten (10) other unrelated “superbug” outbreaks following ERCP, similar in many salient aspects to Advocate Lutheran General Hospital’s CRE outbreak, have been reported within the past few years, both in the U.S. and in Europe, including in France.

And, a study of these more than ten other outbreaks suggests that each may have the same, or a similar, cause, sharing in common:

  • the same type of infectious bacterium: CRE (or a related type of multi-drug resistant gram-negative bacterium);
  • the same identified source: a contaminated GI endoscope; and
  • the same type of medical procedure during which the superbug is transmitted: GI endoscopy, most often ERCP.

Several of these other published examples of transmission of CRE during ERCP (performed both in the U.S. and Europe) are discussed in Dr. Muscarella’s related article: “Investigation and Prevention of Bacterial Outbreaks following Endoscopic Retrograde Cholangiopancreatography” — click here to read it.

Indeed, these several reports suggest that patient-to-patient transmission of CRE during ERCP is, right now, not isolated to one hospital, but a potentially systemic and global public-health concern.

Click here to read Dr. Muscarella’s related article about Lutheran General Hospital’s outbreak: “Overlooked Outbreaks of ‘CRE’ Following GI Endoscopy: A ‘Superbug’ Epidemic in Our Midst?

In addition to Advocate Lutheran General Hospital’s CRE outbreak, which the CDC investigated and wrote about (in the January 3, 2014, issue of MMWR; click here), some of these other more than ten published reports of superbug outbreaks (primarily of CRE outbreaks) include:

1.  Carbonne et al. (2010): Discussing an outbreak following ERCP of KPC-producing K. pneumoniae (type 2) (click here), which is a type of CRE, Carbonne et al. (2010) report that this outbreak:

… highlights the risk of transmitting multidrug-resistant bacteria through endoscopy, particularly through invasive procedures such as duodenoscopy (e.g., ERCP) …  Seven of the 17 patients who underwent endoscopy with the same duodenoscope used for the source case were contaminated with the outbreak strain. — Carbonne et al. (2010)

These authors conclude that a single duodenoscope (that is, a ERCP endoscope) “represented a persistent source of contamination.”

This report is of a multi-hospital outbreak identified in a suburb south of Paris, France, in 2009, with 8 documented cases of infection or colonization with the outbreak’s strain of CRE. No deaths attributed to this outbreak were reported.  Nor did this report mention the specific model and brand of ERCP endoscope linked to this CRE outbreak.


Click here to read Dr. Muscarella’s recent article “GI Endoscopy: Pushed Beyond its Reprocessing Limits?”

2.  Alrabaa et al. (2013): Publishing findings similar to Carbonne et al.’s (2010), Alrabaa et al. (2013) reported that, between June, 2008, and January, 2009, seven (7) patients in Florida (USA) were infected or colonized with KPC-producing K. pneumoniae (a CRE superbug) following ERCP performed at one endoscopy center (shared by two hospitals) (click here).  Infection sites included, as is typical, blood, bile, and urine, and one of these affected patients died during hospitalization.

Consistent with both the CDC’s findings in MMWR (click here) and Carbonne et al.’s (2010) findings (see above), either of which implicates the design of the ERCP endoscope as a likely cause of, or contributing factor to, CRE transmission, Alrabaa et al. (2013) found the suspect GI endoscope’s “elevator area” to be contaminated with carbapenemase-producing E. coli, another type of CRE superbug, due to “inadequate cleaning of the complex terminal part of the ERCP scope.”

Acknowledging that that the ERCP endoscope is particularly difficult to clean because its distal tip features a “small tube with a complex design including a small mobile metal piece called the ‘elevator’,” Alrabaa et al. (2013) conclude that the contaminated GI endoscope itself was the source of this outbreak’s resistant strain of CRE.

According to Alrabaa et al. (2013), the ERCP endoscope’s “elevator piece” was not cleaned in accordance with the manufacturers’ instructions and “needs additional manual cleaning using a brush prior to standard scope processing,” to prevent disease transmission and ensure that this elevator piece does not harbor “dangerous microorganisms,” like the “biodebris” that Alrabaa et al. (2013) found remained under the elevator piece of the implicated scope after it was presumably cleaned.”

Attention – TEE probe contamination:  The Los Angeles County Department of Public Health reported in 2006 a hospital’s outbreak of E. coil respiratory infections due to a reusable probe used to perform transesophageal echocardiography (“TEE”) — click here.

This TEE probe was implicated as the cause of this outbreak for several reasons, including its cracked surface, which — similar to the main article’s discussion of “superbug” outbreaks due to ERCP endoscopes remaining contaminated after reprocessing — may have harbored the outbreak’s bacteria despite cleaning and disinfecting the TEE probe.

The CDC similarly reported that the ERCP endoscope’s distal tip remained contaminated with CRE after presumably having been cleaned and high-level disinfected. The specific model and brand of ERCP endoscope linked to the CRE outbreak reported by Alrabaa et al. (2013) are not mentioned in this report.

3.  Aumeran et al. (2010):  Discussing another outbreak in France, this time in the city of Clermont-Ferrand, Aumeran et al. (2010) report that 16 patients were infected or colonized with multidrug-resistant K. pneumoniae, which is a superbug, following ERCP performed between December, 2008 and August, 2009.

 Click here to read Dr. Muscarella’s accompanying editorial review of Aumeran et al.’s (2010) report.

Reminiscent of the conclusions of the CDC’s report in MMWR and of the findings of both Carbonne et al. (2010) and Alrabaa et al. (2013), above, Aumeran et al. (2010) report that the outbreak’s strain of extended-spectrum beta-lactamase (ESBL)-producing K. pneumoniae “was finally isolated from one duodenoscope (i.e., an ERCP endoscope)” (click here).

Specifically, Aumeran et al. (2010) report that:

  • ERCP endoscopes “can act as a reservoir” for ESBL-producing K. pneumoniae and other types of multi-drug resistant bacteria;
  • contamination of the ERCP endoscopes persisted “despite repeated disinfections”; and
  • ERCP endoscopes are “difficult to clean and disinfect, especially when they have a non-detachable distal tip, which hampers the mechanical removal of the distal debris in the internal channels. Appropriate mechanical flushing and cleaning with detergent of the raiser channel that contains the elevator wire is an essential step for these devices.”

(Note: Dr. Muscarella raised just this possibility of the potential for a non-detachable hood on the ERCP endoscope’s distal tip contributing to Advocate Lutheran General Hospital’s CRE outbreak in another of his articles about Lutheran General Hospital’s outbreak.  See: “Overlooked Outbreaks of ‘CRE’ Following GI Endoscopy: A ‘Superbug’ Epidemic in Our Midst?” — click here. )

ESBL-producing bacteria: Briefly, while ESBL-producing K. pneumoniae is resistant to cephalosporins (e.g. cefuroxime, cefotaxime and ceftazidime), which are the most widely used antibiotics in many hospitals, this multi-drug resistant bacterium remains susceptible to carbapenems (and cephamycins) and, therefore, is not a CRE.  Aumeran et al. (2010) report that the outbreak’s strain of ESBL-producing K. pneumoniae was resistant to all beta-lactam antibiotics except carpapemens.

The types of GI endoscopes used by this hospital in France were reported to be Olympus TJF 140 and 160 models, with the former type being of a design that, according to Aumeran et al. (2010), precludes detachment of the ERCP endoscope’s distal tip, which, according to these authors, “makes mechanical removal of the distal debris in the elevator wire channel more difficult.”

Attention: Aumeran et al. (2010) report that the peracetic acid-based agent used for high-level disinfection of the contaminated ERCP endoscopes (as well as the enzymatic cleaning product used to clean the ERCP endoscopes) “were fully effective against the epidemic strain.”

This finding could raise questions about whether the employment of ethylene oxide (EtO) gas sterilization was as crucial to the termination of Advocate Lutheran General Hospital’s aforementioned CRE outbreak as some reports have suggested.

So, too, could the recent change to the EPA-registration of an intermediate-level disinfectant, which is now labeled to kill  Enterobacter cloacae (NDM-1 positive) and K. pneumoniae (KPC-2 positive, multi-drug and carbapenem resistant) within 2 minutes. These organisms are both CRE, and if intermediate-level disinfection so quickly kills these CRE, certainly the more robust process of high-level disinfection, if performed properly, would be expected to kill easily Advocate Lutheran General Hospital’s outbreak strain of CRE.

4A.  Bajolet et al. (2013) – Part 1:  Bajolet et al. (2013) reported an outbreak at a hospital in Reimes, France, in 2011, following GI endoscopy caused by yet a third type of superbug:  ESBL-producing Pseudomonas aeruginosa.

Whereas ESBL-producing gram-negative superbugs are usually multi-drug bacteria that are resistant to some β-lactam antibiotics, like penicillins and cephalosporins, these superbugs are currently susceptible to carbapenems. CRE (gram-negative) superbugs, in contrast, are resistant to carbapenems, too.

This time, these infections were linked to gastroscopy (not ERCP, although both are upper GI endoscopic procedures). (Note: The other two species of the superbugs recently linked to contaminated ERCP endoscopes are, as mentioned previously, KPC-producing K. pneumoniae and New Delhi Metallo-β-Lactamase–Producing E. coli.)

Referring to this superbug as “MDR-PA” for “multi-drug resistant P. aeruginosa,” Bajolet et al. (2013) isolated this outbreak’s strain from a single gastroscope (which is a type of GI endoscope) that had been used on 182 affected patients.

In addition to having identified some important breaches in the manual cleaning of the gastroscope, Bajolet et al. (2013) report that a minor defect — namely wear of adhesive at the gastroscope’s distal sheath — “may have contributed to the development and persistence of bacterial biofilm in this case.”

This report’s finding that a GI endoscope was contaminated with the outbreak’s strain of the superbug is consistent with the other reports that are discussed above linking CRE transmissions to contaminated GI endoscopes. The specific model and brand of gastroscope linked to this superbug outbreak are not mentioned in this report.

4B.  Bajolet et al. (2013) – Part 2:  Bajolet et al.’s (2013) report raises another important point:  In contrast to Advocate Lutheran General Hospital’s screening of 243 patients (who underwent ERCP during the outbreak between January, 2013, and September, 2013) potentially exposed to the outbreak’s CRE strain, Bajolet et al. (2013) report that none of the 182 affected patients, who were potentially exposed to the contaminated gastroscope used by this hospital in France, in 2011, were notified of this breach and told to return to the hospital to be screened for infection with a bacterial superbug.

Attention Healthcare Facilities: Could your GI endoscopy unit be harboring “superbugs”?  Click here to read about an safety/auditing program specifically designed by Dr. Muscarella – this article’s author – to prevent infection-control breaches and disease transmission during ERCP and other GI endoscopic procedures.

According to Bajolet et al.’s (2013), the rationale for not notifying any of these 182 patients of their possible infection or colonization with the outbreak’s antibiotic-resistant strain of bacteria, while inconsistent with Advocate Lutheran General Hospital’s response to its respective outbreak, was because “neither treatment strategies nor specific precautions exist for colonization with MDR-PA,” which was the outbreak’s bacterial strain.

Whether this rationale is sound could be debated. Nonetheless, that a significant number of Bajolet et al.’s (2013) originally affected 182 patients could be unknowingly colonized or infected today with the outbreak’s superbug strain is unclear, but a potentially concerning possibility that might warrant attention and redress, because according to the CDC, people can remain colonized with a superbug like CRE for months, without knowing it — being, therefore, potential “microbial time bombs” — with these colonizing strains posing an increased risk of infection if they were to enter a sterile body site, such as the urinary tract or the bloodstream.

A mortality rate of as high as 50% is associated with infection of the patient’s bloodstream with the superbug CRE. And, if proper hygiene is not exercised (i.e., proper hand washing), then CRE, which may be found in a person’s stool, could be unwittingly transmitted from one un-screened, colonized person in the community to another through direct and indirect contact.

Dr. Muscarella discusses the possibility of patients who recently underwent ERCP being unknowingly colonized or infected in his article “Lessons Taught by a Recent “Superbug” Outbreak: Could Ex Post Facto Notification be Warranted?” (click here), writing that such notification to ensure eradication of the outbreak’s strain of bacteria could (but would not necessarily) prove crucial to preventing the further spread of person-to-person CRE within the community.

5.  Naas et al. (2010):  And finally, Naas et al. (2010) similarly reported transmission of carbapenem-resistant K. pneumoniae, which produced the KPC-2 β-lactamase enzyme, in France via a contaminated side-viewing duodenoscope (i.e., an ERCP endoscope).

This authors recommend the following measures to prevent transmission of a CRE via a contaminated GI endoscope: (i) prompt reprocessing of the GI endoscope after its use, not as many as 24 hours later during which time patient debris may dry on the endoscopes; (ii) assuring thorough drying of the GI endoscope’s internal channels; and (iii) microbiological sampling of the GI endoscope several times a year, to evaluate it for bacterial contamination.

Conclusions, summary, and recommendations

As a result of a review of the medical literature, a number of points are provided:  First, several recommendations to prevent transmissions of CRE in the healthcare setting, particularly during ERCP, are provided in Dr. Muscarella’s related article “Investigation and Prevention of Bacterial Outbreaks following Endoscopic Retrograde Cholangiopancreatography, or ERCP” — click here to read it.  These previously published recommendations include strict adherence to the manufacturer’s instructions for manually cleaning the area of the ERCP endoscope that houses its elevator forceps.

In addition to Standard Precautions, Contact Precautions are indicated to prevent CRE’s person-to-person transmission. Click here to read Dr. Muscarella article about such “Transmission-based Precautions.”

And, as Naas et al. (2010) recommend (see above), reprocessing the GI endoscope promptly after its clinical use, along with both terminally drying the GI endoscope’s internal channels following reprocessing and frequent microbiological monitoring of the GI endoscope’s channels for contamination are important quality and safety measures designed to prevent a GI endoscope’s transmission of CRE.

Second, the six reviewed reports by the CDC, Alrabaa et al. (2013), Bajolet et al. (2013), Aumeran et al. (2010), Carbonne et al. (2010), and Naas et al. (2010), among others, of recent superbug outbreaks following GI endoscopy display a seemingly hitherto overlooked, yet seemingly troubling trend (note that the number of “reported” instances of CRE transmissions may significantly under-estimate the true incidence of these types of infections):

With significant public-health implications, this review inexorably compels the conclusion that not only are “superbug” (e.g., CRE) outbreaks linked to contaminated GI endoscopes not isolated, rare, or unique to any one hospital, but they are, right now, apparently a systemic problem across the nation, in Europe, and globally.

Third, this review article concludes that the GI endoscope’s physical design may be an important contributing factor to superbug transmissions in the healthcare setting following ERCP, causing this complex reusable instrument itself — with focus placed on the ERCP endoscope’s elevator wire channel, non-removable distal hood, and elevator forceps — to be formidable to clean and high-level disinfect and to be an apparent source or reservoir of several CRE outbreaks following ERCP.

The ERCP endoscope is formidable to clean and high-level disinfect and is an apparent source of several CRE outbreaks recently reported in the U.S. and in Europe, including in France. — Lawrence F Muscarella, PhD

This review article found that ERCP endoscopes, linked to outbreaks of CRE and other types of superbugs, at times remained contaminated despite presumably having been cleaned and high-level disinfected.  Whether ethylene oxide (EtO) gas sterilization is sufficiently robust to reliably and consistently overcome the limitations that the ERCP endoscope’s complex physical design reportedly pose to reprocessing has been suggested — click here to read Dr. Muscarella’s discussion of this topic — but requires more data before a definitive answer can be provided.

Additional reading: A list of several articles by Dr. Muscarella discussing Advocate Lutheran General Hospital’s “superbug” outbreak in 2013 are listed on this page for the reader’s convenience.

Also requiring more research is whether, as the several reports of CRE outbreaks reviewed herein suggest, the GI endoscope’s complex physical design, including the ERCP endoscope’s elevator forceps, is itself the “smoking gun,” or primary cause, of these documented instances of CRE transmissions following GI endoscopy.  The fact that another hitherto unrecognized factor unrelated to the ERCP endoscope’s design may, too, have contributed to causing one or more of these CRE outbreaks seems plausible and cannot necessarily be ruled out at this time (see next section, below).

And, fourth, as Aumeran et al. (2010) wisely instruct, more public reporting, monitoring and investigations of superbug outbreaks linked to GI endoscopes are necessary to better understand all of their possible causes, which seemingly include, in summary, unsuccessful cleaning and high-level disinfection of GI endoscopes, due to their complex design.

Opaqueness, on the other hand — namely, a hospital’s reluctance to disclose an outbreak of CRE (or another superbug) encountered in one of its departments, due to a fear of causing the public to lose confidence in the quality of care — can increase the likelihood of the resistant bacterium’s spread.

According to Dr. Lynora Saxinger (click here), an infectious diseases specialist at the University of Alberta in Edmonton, a culture of safety, information about CRE outbreaks and how the risk of infection are being managed requires open communication.

Often these outbreaks may be occurring and we don’t even know about them.” — Dr. Michael Gardam, an infectious disease specialist at Toronto General Hospital (click here).

Immediate attention and the prompt implementation of additional corrective actions and improved procedures validated for the prevention of CRE transmission following GI endoscopy is recommended.

An unresolved issue: CRE-contaminated rinse water?

The possibility remains that an unrecognized factor may have contributed to Advocate Lutheran General Hospital’s CRE outbreak in 2013.  To be sure, the CDC’s MMWR report (January 3, 2014) does not discuss whether the CDC or hospital officials microbiologically sampled the hospital’s tap water, or the rinse water used by the hospital’s automated endoscope reprocessor (AER), to exclude, or to confirm, either as a possible source of this hospital’s CRE outbreak.

According to the CDC, the implementation of EtO gas sterilization for processing Advocate Lutheran General Hospital’s ERCP endoscopes stopped its CRE outbreak, but this outcome may have been due as much to EtO gas’s sterilizing effectiveness as to it being, unlike the AER’s high-level disinfecting process, an entirely “dry” process.

Interestingly, a report by Kotsanas et al. (2013) describe an investigation that identified the likely source of a CRE outbreak in an intensive care unit (ICU) to be contaminated sinks.  Three clinical isolates of the CRE’s outbreak strain (i.e., Serratia marcescens that produces carbapenemases) were indistinguishable or closely related to four environmental isolates sampled from the grates and drains of several hand-washing sinks located in the ICU.

According to Kotsanas et al. (2013), first, CRE can be “hardy” environmental organisms that develop and grow in biofilms; and, second, their findings demonstrate the key role that bacterial contamination of the environment can play in the transmission of CRE in the healthcare setting.

Similarly, Starlander and Melhus (2012) reported that during a period of seven months, four patients in a neurosurgical ICU became infected or colonized by a multi-drug resistant strain of K. pneumoniae.  The investigation revealed that the source of this outbreak was a contaminated sink. This outbreak was successfully controlled, in part, by replacing the sink and its plumbing.

And, Walsh and colleagues (2011) identified NDM-1-positive bacteria in samples of drinking water and waste seepage in Asia. In short, therefore, the type of CRE recently confirmed to be responsible for an outbreak at a hospital near Chicago, IL, in 2013 following ERCP — click here to read more about this outbreak — is not exclusively a patient-borne bacterium.

Muscarella (2004), too, has written about the contribution of the environment to outbreaks of antibiotic-resistant gram-negative bacteria.

In his paper Muscarella (2004) asked whether the cause of an outbreak of imipenem-resistant P. aeruginosa following bronchoscopy, which was investigated by Sorin et al. (2001), might have been due more to bacterial contamination of the water used to rinse the bronchoscope after its chemical reprocessing (coupled with inadequate terminal forced-air drying of the bronchoscope) than, as suggested by Sorin et al. (2001), patient-to-patient transmission due to the improper connection of an automated endoscope reprocessor to the bronchoscope.

In another paper Muscarella (2010) discusses the potential contribution of environmental surfaces to outbreaks of multidrug-resistant K. pneumoniae, emphasizing that these surfaces, including rinse water, should not be excluded as plausible sources of ERCP-related infections of ordinarily enteric bacteria, including those that are resistant to antibiotics, unless patient-to-patient transmission has been definitively confirmed.

Other instances during the past 30 years linking patient morbidity and mortality to ERCP endoscopes terminally rinsed with contaminated water during their reprocessing have been published (Muscarella, 2004). Whether Advocate Lutheran General Hospital’s CRE outbreak in 2013 could have been due to contaminated rinse water — not inadequate cleaning or high-level disinfection of the ERCP endoscope, per se, due to the ERCP endoscope’s complex physical design as intimated by the CDC in its January 3, 2014, issue of MMWR — remains unclear, but available data, to date, do not rule out this possibility.

Indeed, rinse water contaminated with CRE being a possible “smoking gun” reponsible for Advocate Lutheran General Hospital’s outbreak in 2013 would also be consistent with the recent publication of data (see above) showing (via an EPA-registration) that even intermediate-level disinfection — and therefore, certainly, high-level disinfection — destroys tested strains of CRE within 2 minutes.  It could be that high-level disinfection of Advocate Lutheran General Hospital’s ERCP endoscopes was effective, but was compromised with contaminated water during endoscope-reprocessing’s subsequent water-rinse phase.

Attention Healthcare Facilities:  Contact Dr. Muscarella in strict confidence – click here – if you have any questions about a possible outbreak of bacteria linked to a contaminated endoscope. (Click here to read more about Dr. Muscarella’s program for auditing the safety and quality of healthcare facilities.)


  1. Alrabaa SF, Nguyen P, Sanderson R, et al. Early identification and control of carbapenemase-producing Klebsiella pneumoniae, originating from contaminated endoscopic equipment. Am J Infect Control 2013 Jun;41(6):562-4.
  2. Aumeran C, Poincloux L, Souweine B, et al. Multidrug-resistant Klebsiella pneumoniae outbreak after endoscopic retrograde cholangiopancreatography. Endoscopy 2010 Nov;42(11):895-9.
  3. Bajolet O, Ciocan D, Vallet C. et al. Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa. J Hosp Infect 2013 Apr;83(4):341-3.
  4. Carbonne A, Thiolet JM, Fournier S, et al. Surveillance and outbreak reports Control of a multi-hospital outbreak of KPC-producing Klebsiella pneumoniae type 2 in France, September to October 2009. Euro Surveill 2010 December 2;15(48):pii=19734 (click here).
  5. Centers for Disease Control and Prevention (CDC). Notes from the Field: New Delhi Metallo-β-Lactamase–Producing Escherichia coli associated with endoscopic retrograde cholangiopancreatography — Illinois, 2013. MMWR January 3, 2014;1051 (click here).
  6. Kotsanas D, Wijesooriya W, Korman T, et al. “Down the drain”: carbapenem-resistant bacteria in intensive care unit patients
    and hand-washing sinks. MJA 2013; 198: 267–269.
  7. Muscarella LF. Contribution of tap water and environmental surfaces to nosocomial transmission of antibiotic-resistant Pseudomonas aeruginosa. Infect Control Hosp Epidemiol 2004 Apr;25(4):342-5.
  8. Muscarella LF. Investigation and prevention of infectious outbreaks during endoscopic retrograde cholangiopancreatography. Endoscopy 2010 Nov;42(11):957-9.
  9. Naas T, Cuzon G, Babics A, et al. Endoscopy-associated transmission of carbapenem-resistant Klebsiella pneumoniae producing KPC-2 b-lactamase. J Antimicrob Chemother 2010;1305-6.
  10. Sorin M, Segal-Maurer S, Mariano N, et al. Nosocomial transmission of imipenem-resistant Pseudomonas aeruginosa following bronchoscopy associated with improper connection to the Steris System 1 processor. Infect Control Hosp Epidemiol 2001 Jul;22(7):409-13.
  11. Starlander G, Melhus A. Minor outbreak of extended-spectrum β-lactamase-producing Klebsiella pneumoniae in an intensive care unit due to a contaminated sink. J Hosp Infect 2012 Oct;82(2):122-4.
  12. Walsh TR et al. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: An environmental point prevalence study. Lancet Infect Dis 2011;11:355.

Article by: Lawrence F Muscarella, PhD, president and owner of the think-tank quality and safety company “LFM Healthcare Solutions” — click here for a list of its services.  Article posted 1/30/2014; updated 10/29/2014, Rev A.

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